Hypotheses that didnt float

In the history of the study of ornithopods, habitats and anatomy conspired to put some of these animals in exotic places and give them unusual locomotor skills. For example, hadrosaurids were once regarded as amphibious, in part because the tail was long and deep (great for sculling in the water), the hand ap peared webbed, and the jaws were deemed too weak to handle anything but soft aquatic vegetation. Not true in all three cases. In a similar fashion, for over 100 years, a species of HypsWo-phodon was regarded as a tree-dweller. Upon close scrutiny by University ofBridgeport paleontologist P. M. Galton (see Figure 14.10b), however, this animal was found to have no specializations for this particularly demanding mode of life.

The combination of a strongly seasonal African habitat and some basic heterodontosaurid anatomy created a dilemma - and ultimately a solution - for A. R. Thulborn (University of Queensland), in 1978. Heterodontosaurids, he believed, chewed by moving the lower jaw forward and backward relative to the upper jaw. Yet evidence of tooth replacement that he expected (given that heterodontosaurids fed on very abrasive food) simply did not exist. To replace the teeth gradually would have impaired their ability to feed, he reasoned, so the teeth could only have been replaced en masse. How could this be accomplished? Thulborn argued that heterodontosaurids must have estivated (lay dormant), most likely during the dry season. While dormant, the formerly functional teeth fell out and were replaced, to be worn down while the animal was active and feeding during each wet season.

Several years after Thulborn's estivation hypothesis had appeared, the University of Chicago's J. A. Hopson re-examined heterodontosaurid jaw mechanics and tooth replacement patterns. As it turns out, heterodontosaurids chewed transversely, not forward and backward, so that tooth replacement was reduced, but not lost, in these animals. The combination ofthese two aspects of heterodontosaurid feeding are mutually compatible and certainly do not call for periods of dormancy to accommodate rapid tooth replacement. Thus anatomical support for Thulborn's hypothesis disappeared. There is no compelling reason to believe that heterodontosaurids engaged in estivation during the harshness ofthe southern African climate of the Early Jurassic.

Many iguanodontians had very specialized fingers and hands, indicating multiple functions (Figure 7.6). In Iguanodon, for example, the first digit (thumb) was conical and sharply pointed. It has been suggested that it was used as a stiletto-like, close-range defensive weapon or for breaking into seeds and fruits (or both, or . . . ?). The middle digits (II, III, and IV) were tipped with hooves, and were evidently weight-bearing; these would have been key players when the animal was in a quadrupedal stance. Finally, the outer finger (V) was highly flexible, and could bend across the palm, very much as the thumb does in humans - a grasping, opposable pinkie.

Unlike other iguanodontians, in hadrosaurids digit I of the hand was lost, and digit V was relatively small. This left three main fingers, all tipped with hooves, with hardly any way to function other than to support the animal while standing. Hadrosaurids likely spent a lot of time on all fours.

Dietary fiber. Fine dining, ornithopod style, is relatively well understood. For hadrosaurids at least, "mummies," complete with stomach contents, have been found. These spectacular

Figure 7.6. The hand of Iguanodon. Note the spiked thumb (digit I).

specimens, though not true mummies in the sense that original soft tissue and bone are preserved, apparently first dried to dinosaur jerky before burial. The dried, toughened muscle and flesh tissue didn't decompose, so the whole package - tissue and bones - was replaced during burial (see Chapter 1). The startling result is preserved skin impressions, stretched tendons and muscles, and the last supper in the stomach and intestines. Hadrosaurids, we now know, ate twigs, berries and coarse plant matter.

This selection of food correlates nicely with ornithopod height: they are thought to have been active foragers on ground cover and low-level foliage from conifers and in some cases from deciduous shrubs and trees of the newly evolved angiosperms; that is, the clade of all plants that bear flowers (see Chapter 13). Browsing on such vegetation appears to have been concentrated within the first meter or two above the ground, but the taller animals may have reached vegetation as high as 4 m.

Eating coarse, fibrous food requires some no-nonsense equipment in the jaw to extract enough nutrition for survival, and ornithopods had the necessary goods (Figures 7.7, 7.8, and 7.9). Like all genasaurs, ornithopods had a beak in the front for cropping vegetation, a diastema, a group of cheek teeth for shearing (Figure 7.10), and a large, robust coronoid

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30 cm process for serious mastication. A deeply inset tooth row indicates large fleshy cheeks. But beyond these basics, different ornithopods had different modifications of the jaw, and different kinds of jaw motions are believed to have been used for the processing of food.

Modern treatments of ornithopod jaw mechanics suggest some differences in ornitho-pod feeding behavior. In basal ornithopods, the beak was relatively narrow, implying a somewhat selective cropping ability. Euornithopods, by contrast, had broad snouts (Figure 7.11), and in some cases even developed a strongly serrated edge on the rhamphotheca. They were likely not too selective; instead, they hacked and severed leaves and branches without much regard for what they were taking in. Basal ornithopods were likely careful nibblers, while euornithopods were lawn-mowers.

Beyond the diastem, the chewing began. Here it was aided by something that is utterly foreign to humans. Our skulls and lower jaws are akinetic, meaning that, except for the vertical motion of the lower jaws, the bones in our skulls are solidly fused and locked together. Not so with ornithopods. Above and beyond the familiar up and down compression

20 cm of chewing, slight movements of particular, individual bones within the skull and lower jaws allowed the cheek teeth to grind past each other from side to side. A skull in which individual bones move is called kinetic.

Euornithopods evolved a unique, kinetic skull, in which they mobilized their upper jaws. This kind of mechanism, called pleurokinesis, involved a slight outward rotation of portions of the upper jaw, especially the maxilla (the bone that contains the upper teeth), with each bite (Figure 7.12). When the upper and lower teeth were brought into contact on both right and left sides, the opposing surfaces of the dental batteries sheared past one another. Pleurokinesis was an important advance for euornithopods, giving them the ability to chew the toughest, most fibrous plants.

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Figure 7.10. Upper tooth of (a) Lycorhinus, (b) upper tooth of Hypsilophodon, (c) three upper teeth of Iguanodon, and (d) lower dental battery of Lambeosaurus. Note that the teeth in these forms are progressively more tightly packed, culminating in the lambeosaur dental battery.

Chewing reached its most refined state in hadrosaurids, in which the cheek teeth were fitted tightly together into a dental battery, which effectively acted as a single shearing or grinding tool in each jaw (see Figure 7.10d). With constantly replacing teeth, tooth wear was never an issue (as it is in mammals, which only replace teeth once so that their adult teeth have to last their entire lives). The toughest, most fibrous plants undoubtedly succumbed to the hadrosaurid combination of powerful jaw muscles operating on a pleurokinetic skull equipped with constantly replaced grinding surfaces.

As in all of the other ornithischians that have been discussed, once the food was properly chewed, it was swallowed, and quickly passed through a capacious gut that was present in all ornithopods, and proportionately even larger in the largest iguanodontians (including hadro-saurs). Ornithopods were uniquely equipped to extract the most nutrition out of a low-quality, high-fiber, high-volume diet.

Thoughts of an ornithopod. By dinosaur standards, ornithopods were smart - as smart or smarter than might be expected of living archosaurs if they were scaled up to dinosaur size (see Box 12.4). For example, Leaellynasaura, a basal euornitho-pod from Victoria, Australia, was apparently quite brainy and had acute vision, as suggested by prominent optic lobes in the brain.1 In general, ornithopod smarts may be related to greater reliance on sight, smell, and hearing for protection that, in the absence of other means, may have been their only defense. Moreover, brain size in these dinosaurs may have also been an integral part of a complex behavioral repertoire.

Figure 7.11. Edmontosaurus, a flat-headed hadrosaurid from the western USA.

Socializing a la Ornithopoda

From the time of their discovery, ornithopods have attracted a good deal of attention, particularly for the extraordinary crests on the heads of hadrosaurids and the lumps on the forehead of Ouranosaurus. All of these features hint at sophisticated social behavior.

Song of the saurian. Hadrosaurids have attracted the most attention, in large part because of the striking solid or hollow crests - many of them chambered - borne by many genera. The hollow crest morphology was once thought to relate to the aquatic habits of the group (see Box 7.1) or to smell, but studies suggest that the internal chambers of the crests would

1. The animal had an estimated encephalization quotient (EQ; see Box 12.4) of 1.8; J. A. Hopson estimated that the average EQ of other ornithopods is about 1.5.

have made good resonating chambers, producing loud, low-frequency sounds - a kind of Mesozoic alpenhorn. With that insight, much of the discussion now centers on intraspecific competition (see Chapter 5) and sexual selection (see Chapter 6). To convey information about species, sex, and even rank, crests had to have been visually and, if part of their function was as a resonating chamber, vocally distinctive. Only then can they have promoted successful matings between consenting adults. How strongly is the role of sexual selection implied by hadrosaurid crests?

Paleontologist J. A. Hopson made five predictions that test the hypothesis that hadro-saurid crest morphology was all about sexual selection.

1. If communication and display were important, hadrosaurids must have had both good hearing and good vision.

2. If the crest served the dual role of visual display and as a vocal resonator, then its external shape need not necessarily mimic the internal shape of the resonating cavities inside.

3. If crests acted as visual signals, then they should be species-specific in size and shape, and they should also be sexually dimorphic.

4. If the crests were a visual cue, they ought to be increasingly distinctive as the number of hadrosaurids living together increases.

5. The crests should become more distinctive through time as a consequence of sexual selection.

How did these hypotheses fare? Hypothesis (1) is relatively well supported, in that hadrosaurids, to judge from their sclerotic rings (see Figure 4.6), had relatively large eyes, implying acute vision. Similarly, preserved middle and inner ear structures suggest that a wide range of frequencies was audible to these animals. Hypothesis (2) is upheld in virtually all cases, in that the profile of the crest is more elaborate or extensive than the walls of the internal plumbing (Figure 7.13). Hypothesis (3) is amply upheld in large part thanks to studies on the growth and development in lambeosaurine hadrosaurids, which show that crests become most prominent when an animal approaches sexual maturity (Figure 7.14). Moreover, adult lambeosaurines are known to be dimorphic, particularly in terms of crest size and shape. Could these "morphs" have been male and female?

Hypothesis (4) is based on the idea that distinctiveness would be an advantage during the breeding season. It was tested at Dinosaur Provincial Park in Alberta, Canada, where five distinctively equipped species of hollow-crested hadrosaurid and one species of solid-crested hadrosaurid all lived together in multi-species bliss. In support of the hypothesis, elsewhere where hadrosaurid diversity is lower, the distinctiveness of the crests is decreased. Interestingly, however, hypothesis (5) is not well supported, for lambeosaurines crests, at least, arguably become less distinctive over time.

If the crests were used for species recognition, ritualized display, courtship, parent-offspring communication, and social ranking, the accentuated nasal arch seen in Gryposaurus, Maiasaura, and Brachylophosaurus may have been used for broadside or head pushing during male-male combat (Figure 7.14). Inflatable flaps of skin possibly covered the nostrils and surrounding regions (Figure 7.15); if present, these could have been inflated and used for visual display, as well as noise-making - more a Mesozoic bagpipe (Figure 7.15b). In Prosaurolophus and Saurolophus (see Figure 7.8f), a sac might have extended onto the solid crest that extended above the eyes (Figure 7.15c), while in Edmontosaurus (see Figures 7.8g and 7.11), where the nasal arch is not accentuated nor is there a crest, the complexly excavated nostril region may have housed an inflatable sac. Unfortunately, these soft-tissue-based hypotheses are all speculative.

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Figure 7.15. (a) The circumnarial depression in Gryposaurus (indicated by cross-hatched region) which may have supported an inflatable flap of skin in hadrosauridines; (b) speculative reconstruction of an inflatable sac in Gryposaurus; (c) speculative reconstruction of an inflatable sac in the solid-crested hadrosaurid Saurolophus.

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In lambeosaurine (hollow-crested) hadrosaurids, the crests perched atop the head must have provided for instant recognition (Figures 7.9 and 7.16). This would have been by visual cues as well as by low honking tones produced in the large resonating chamber of the crest (see Figure 7.13).

Other ornithopods. Other ornithopods show features potentially interpretable in terms of sexual selection and intraspecific competition. Low, broad bumps on top of the head of

Ouranosaurus and the arched snout of Muttaburrasaurus and Altirhinus may well have behavioral significance relating to intraspecific competition and sexual selection. Ouranosaurus was equipped with extremely tall neural spines, which formed a high, almost sail-like ridge down its back (Figure 7.17). Like Stegosaurus (see Chapter 5), it is possible that these long spines were covered with skin and used by the animal to warm up and cool down, and/or they may also have had a display function, providing the animal with a greater side profile than it would otherwise have had.

Display behavior in many ornithopods begins to make even more sense when considered in the context of the discoveries of bonebeds containing just one type of dinosaur. Monotypic

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bonebeds, that is bonebeds containing only one type of animal, are known for Dryosaurus, Iguanodon, Maiasaura, and Hypacrosaurus, among ornithopods. In the case of hadrosaurids, at least, the evidence suggests that a single herd could have exceeded 10,000 individuals, rivaling the multiple mile-sized bison herds that roamed the Great Plains of North America before the unfortunate pairing of the transcontinental railroad with the Winchester rifle.

Bringing up baby II. The secrets of ornithopod reproductive behavior are just beginning to be told. For the small, basal ornithopod Orodromeus, hatchlings had well-developed limb bones, with fully formed joints, indicating that the young could walk, run, jump, and forage for themselves as well as any adult. We thus infer minimal parental care.

As first discovered by paleontologist J. R. Horner, hadrosaurids did not take so laissez-faire an attitude toward child-rearing. Maiasaura, Hypacrosaurus, and probably most others nested in colonies, digging a shallow hole in soft sediments and laying, in the case of Maiasaura, up to 17 eggs in each nest. These nests were separated by about a mother's body length, strongly suggesting that they were regularly tended by a parent. Hatchlings (Figure 7.18) are found amid an abundance of eggshell fragments, implying an extended stay at the nest that wreaked havoc on the eggs that once housed them.

With poorly developed joints and limbs, the offspring were literally helpless during the nest-bound time. They could hardly have foraged far from the nest and must have depended on their parents to provision and protect them. But to go from a 1 m hatchling to a 9 m adult, growth must have come hot and heavy; at approximately 12 cm per month, as fast or faster than fast-growing mammals and birds (see Chapter 12). This means that hatchlings must have channeled into growth virtually all of the food that their parents brought them.

A new take on ornithopod child-rearing was provided by the hypsilophodont Oryctodromeus, a dinosaur that evidently raised atricial young in a burrow (see Figure 1.8). Only one specimen of the animal is known, but this reveals a burrow with an end chamber, in which were found the remains of an adult and two juveniles. Oryctodromeus appears to have some digging specializations in its skull and thoracic region, suggesting a fossorial, or burrowing lifestyle.

Ornithopod life, therefore, certainly involved much opportunity for interaction: within herds, as breeding pairs, and as families. All of this is part and parcel of the visual and vocal communication we postulated earlier, and affirms complex social behavior particularly in hadrosaurids.

Figure 7.18. Left lateral view of the skull and skeleton of a hatchling hadro-saurid Maiasaura.

Ornithopods give us insights into dinosaurian life history strategies; that is, the ways in which particular organisms grow, reproduce, and die. One strategy, called the r-strategy, is to produce enormous numbers of eggs that result in thousands of offspring, the vast majority of which do not survive to reproduce during their relatively short lifespans. Think mayflies. Such offspring, born as near-adults, are called precocial. No parental care here - too many children for serious parental investment.

This contrasts with the K-strategy, involving fewer offspring, lots of parental care, and longer lifespans. Think whales. Such offspring, born with a longer trek toward adulthood and requiring parental investment to get there, are called altricial.

How do those ornithopods for which we have information conform to either of these two contrasting strategies? Orodromeus seems to have been an r-strategist, an inference that is based on the precocial nature of the young. In contrast, Maiasaura, Hypacrosaurus, and perhaps other hadrosaurids had nest-bound, altricial hatchlings, and were likely K-strategists.

The basal split of Ornithopoda from the generalized cerapodan condition likely occurred in the latest Triassic or earliest Jurassic. The clade is diagnosed on the basis of a number of derived features (see Figure 7.5). As we've seen, an early split in Ornithopoda occurred between primitive ornithopods such as Agilisaurus and Euornithopoda (see Figure 7.5), with euornithopods containing much of the future diversity of the clade.

Heterodontosaurids, basal ornithopods, evolved teeth bearing a high, chisel-shaped crown ornamented with denticles. In addition, and the principal basis for the name "hetero-dontosaurid," a large canine-like tooth is present in both upper and lower jaws.

Euornithopoda is a well-diagnosed group (Figure 7.19). It consists of a host of relatively small, agile ornithopods such as Hypsilophodon, and Gasparinisaura, as well as a few